Abstract

The physical basis of flagellar and ciliary beating is a major problem in biology which is still far from completely understood. The fundamental cytoskeleton structure of cilia and flagella is the axoneme, a cylindrical array of microtubule doublets connected by passive cross-linkers and dynein motor proteins. The complex interplay of these elements leads to the generation of self-organized bending waves. Although many mathematical models have been proposed to understand this process, few attempts have been made to assess the role of dyneins on the nonlinear nature of the axoneme. Here, we investigate the nonlinear dynamics of flagella by considering an axonemal sliding control mechanism for dynein activity. This approach unveils the nonlinear selection of the oscillation amplitudes, which are typically either missed or prescribed in mathematical models. The explicit set of nonlinear equations are derived and solved numerically. Our analysis reveals the spatio-temporal dynamics of dynein populations and flagellum shape for different regimes of motor activity, medium viscosity and flagellum elasticity. Unstable modes saturate via the coupling of dynein kinetics and flagellum shape without the need of invoking a nonlinear axonemal response. Hence, our work reveals a novel mechanism for the saturation of unstable modes in axonemal beating.

Highlights

  • Cilia and flagella play a crucial role in the survival, development, cell feeding and reproduction of micro-organisms [1]

  • Our analysis reveals the spatio-temporal dynamics of dynein populations and flagellum shape for different regimes of motor activity, medium viscosity and flagellum elasticity

  • We presented a theoretical framework for planar axonemal beating by formulating a full set of nonlinear equations to test how flagellar amplitude and shape vary with dynein activity

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Summary

Introduction

Cilia and flagella play a crucial role in the survival, development, cell feeding and reproduction of micro-organisms [1]. Other studies examined the dynamics of flagellar beating by prescribing its internal activity [17,18] or by considering a self-organized mechanism independent of the specific molecular details underlying the collective action of dyneins [13,14,19] The latter approach, general from a physics perspective, does not explicitly incorporate dynein kinetics along the flagellum, which has been shown to be crucial in order to understand experimental observations on sperm flagella [20,21,22]. Bending initiation and transient dynamics are studied subject to different initial conditions

Continuum flagella equations
Parameter values
Linear stability analysis
Nonlinear flagellar dynamics
Principal component analysis
Bending initiation and transient dynamics
Findings
Discussion
Full Text
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